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Superoxide generated in the chloroplast stroma causes photoinhibition of photosystem I in the shade-establishing tree species Psychotria henryi

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Abstract

Our previous studies indicated that high light induced significant photoinhibition of photosystem I (PSI) in the shade-establishing tree species Psychotria henryi. However, the underlying mechanism has not been fully clarified. In the present study, in order to investigate the mechanism of PSI photoinhibition in P. henryi, we treated detached leaves with constant high light in the presence of methyl viologen (MV) or a soluble α-tocopherol analog, 2,2,5,7,8-pentamethyl-6-chromanol (PMC). We found that MV significantly depressed photochemical quantum yields in PSI and PSII when compared to PMC. On condition that no PSI photoinhibition happened, although cyclic electron flow (CEF) was abolished in the MV-treated samples, P700 oxidation ratio was maintain at higher levels than the PMC-treated samples. In the presence of PMC, PSI photoinhibition little changed but PSII photoinhibition was significantly alleviated. Importantly, PSI photoinhibition was largely accelerated in the presence of MV, which stimulates the production of superoxide and subsequently other reactive oxygen species at the chloroplast stroma by accepting electrons from PSI. Furthermore, MV largely aggravated PSII photoinhibition when compared to control. These results suggest that high P700 oxidation ratio cannot prevent PSI photoinhibition in P. henryi. Furthermore, the superoxide produced in the chloroplast stroma is critical for PSI photoinhibition in the higher plant P. henryi, which is opposite to the mechanism underlying PSI photoinhibition in Arabidopsis thaliana and spinach. These findings highlight a new mechanism of PSI photoinhibition in higher plants.

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Abbreviations

CEF:

Cyclic electron flow

ETR:

Electron transport rate

F v /F m :

The maximum quantum yield of PSII after dark adaptation

MV:

Methyl viologen

1O2 :

Singlet oxygen

O2 − :

Superoxide

PSI:

Photosystem I

PSII:

Photosystem II

P m :

The maximum photo-oxidizable P700

PMC:

2,2,5,7,8-pentamethyl-6-chromanol

PPFD:

Photosynthetic photon flux density

ROS:

Reactive oxygen species

Y(I):

Quantum yield of PSI

Y(II):

Effective quantum yield of PSII

Y(NA):

The fraction of P700 that cannot be oxidized by a saturation pulse to the overall P700

Y(ND):

The fraction of P700 that is oxidized by actinic light to the overall P700

Y(NO):

Quantum yield of non-regulated energy dissipation at PSII centers

Y(NPQ):

Quantum yield of regulated energy dissipation at PSII centers

References

  • Allahverdiyeva Y, Mamedov F, Mäenpää P, Vass I, Aro EM (2005) Modulation of photosynthetic electron transport in the absence of terminal electron acceptors: Characterization of the rbcL deletion mutant of tobacco. Biochim Biophys Acta 1709:69–83

    Article  CAS  PubMed  Google Scholar 

  • Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophy Acta 1143:113–134

    Article  CAS  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier Science Publishers, Amsterdam, pp 227–287

    Google Scholar 

  • Babbs CF, Pham JA, Coolbaugh RC (1989) Lethal hydroxyl radical production in paraquat-treated plants. Plant Physiol 90:1267–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66

    Article  CAS  PubMed  Google Scholar 

  • Barth C, Krause GH, Winter K (2001) Responses of photosystem I compared with photosystem II to high-light stress in tropical shade and sun leaves. Plant Cell Environ 24:163–176

    Article  CAS  Google Scholar 

  • Bondarava N, Gross CM, Mubarakshina M, Golecki JR, Johnson GN, Krieger-Liszkay A (2010) Putative function of cytochrome b559 as a plastoquinol oxidase. Physiol Plant 138:463–473

    Article  CAS  PubMed  Google Scholar 

  • Brestic M, Cornic G, Fryer MJ, Baker NR (1995) Does photorespiration protect the photosynthetic apparatus in French bean leaves from photoinhibition during drought stress? Planta 196:450–457

    Article  CAS  Google Scholar 

  • Brestic M, Zivcak M, Kunderlikova K, Sytar O, Shao H, Kalaji HM, Allakhverdiev SI (2015) Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. Photosynth Res 125:151–166

    Article  CAS  PubMed  Google Scholar 

  • DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schünemann D, Finazzi G, Joliot P, Barbato R, Leister D (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132:273–285

    Article  CAS  PubMed  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophy Acta 99:87–92

    Article  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Grieco M, Tikkanen M, Paakkarinen V, Kangasjärvi S, Aro EM (2012) Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I under fluctuating white light. Plant Physiol 160:1896–1910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81

    Article  CAS  PubMed  Google Scholar 

  • Hideg É, Kós PB, Vass I (2007) Photosystem II damage induced by chemically generated singlet oxygen in tobacco leaves. Physiol Plant 131:33–40

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Zhang SB, Cao KF (2010a) The different effects of chilling stress under moderate illumination on photosystem II compared with photosystem I and subsequent recovery in tropical tree species. Photosynth Res 103:175–182

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Zhang SB, Cao KF (2010b) Stimulation of cyclic electron flow during recovery after chilling-induced photoinhibition of PSII. Plant Cell Physiol 51:1922–1928

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Zhang SB, Zhang JL, Hu H (2015) Photoinhibition of photosystem I under high light in the shade-established tropical tree species Psychotria rubra. Front Plant Sci 6:801

    PubMed  PubMed Central  Google Scholar 

  • Huang W, Yang YJ, Hu H, Zhang SB (2016a) Moderate photoinhibition of photosystem II protects photosystem I from photodamage at chilling stress in tobacco leaves. Front Plant Sci 7:182

    PubMed  PubMed Central  Google Scholar 

  • Huang W, Yang YJ, Zhang JL, Hu H, Zhang SB (2016b) PSI photoinhibition is more related to electron transfer from PSII to PSI rather than PSI redox state in Psychotria rubra. Photosynth Res 129:85–92

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Yang YJ, Hu H, Zhang SB (2016c) Responses of photosystem I compared with photosystem II to fluctuating light in the shade-establishing tropical tree species Psychotria henryi. Front Plant Sci 7:1549

    PubMed  PubMed Central  Google Scholar 

  • Kitao M, Lei TT, Koike T, Tobita H, Muruyama Y (2000) Susceptibility to photoinhibition of three deciduous broadleaf tree species with different successional traits raised under various light regimes. Plant Cell Environ 23:81–89

    Article  Google Scholar 

  • Klüghammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192:261–268

    Article  Google Scholar 

  • Klüghammer C, Schreiber U (2008) Saturation pulse method for assessment of energy conversion in PSI. PAM Application Notes (PAN) 1:11–14

    Google Scholar 

  • Kojima K, Oshita M, Nanjo Y, Kasai K, Tozawa Y, Hayashi H, Nishiyama Y (2007) Oxidation of elongation factor G inhibits the synthesis of the D1 protein of photosystem II. Mol Microbiol 65:936–947

    Article  CAS  PubMed  Google Scholar 

  • Kono M, Noguchi K, Terashima I (2014) Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant Cell Physiol 55:990–1004

    Article  CAS  PubMed  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  CAS  PubMed  Google Scholar 

  • Krause GH, Grube E, Koroleva OY, Barth C, Winter K (2004) Do mature shade leaves of tropical tree seedlings acclimate to high sunlight and UV radiation? Funct Plant Biol 31:743–756

    Article  Google Scholar 

  • Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346

    Article  CAS  PubMed  Google Scholar 

  • Maurino VG, Peterhansel C (2010) Photorespiration: current status and approaches for metabolic engineering. Curr Opin Plant Biol 13:249–256

    Article  PubMed  Google Scholar 

  • Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4:130–135

    Article  CAS  PubMed  Google Scholar 

  • Miyake C, Horiguchi S, Makino A, Shinzaki Y, Yamamoto H, Tomizawa K (2005) Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of Chl fluorescence in tobacco leaves. Plant Cell Physiol 46:1819–1830

    Article  CAS  PubMed  Google Scholar 

  • Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371

    Article  CAS  PubMed  Google Scholar 

  • Munekage Y, Hashimoto M, Miyake C, Tomizawa KI, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46

    Article  CAS  PubMed  Google Scholar 

  • Oelze ML, Vogel MO, Alsharafa K, Kahmann U, Viehhauser A, Maurino VG, Dietz KJ (2011) Efficient acclimation of the chloroplast antioxidant defence of Arabidopsis thaliana leaves in response to a 10-or 100-fold light increment and the possible involvement of retrograde signals. J Exp Bot 63:1297–1313

    Article  PubMed  PubMed Central  Google Scholar 

  • Sejima T, Takagi D, Fukayama H, Makino A, Miyake C (2014) Repetitive short-pulse light mainly inactivates photosystem I in sunflower leaves. Plant Cell Physiol 55:1184–1193

    Article  CAS  PubMed  Google Scholar 

  • Sonoike K, Terashima I, Iwaki M, Itoh S (1995) Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. FEBS Lett 362:235–238

    Article  CAS  PubMed  Google Scholar 

  • Suorsa M (2015) Cyclic electron flow provides acclimatory plasticity for the photosynthetic machinery under various environmental conditions and developmental stages. Front Plant Sci 6:800

    Article  PubMed  PubMed Central  Google Scholar 

  • Suorsa M, Jarvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjarvi S, Paakkarinen V, Tikkanen M, Jansson S, Aro EM (2012) PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24:2934–2948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takagi D, Takumi S, Hashiguchi M, Sejima T, Miyake C (2016) Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition. Plant Physiol 171:1626–1634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terashima I, Funayama S, Sonoike K (1994) The site of photoinhibition in leaves of Cucumis-sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193:300–306

    Article  CAS  Google Scholar 

  • Tikkanen M, Aro EM (2014) Integrative regulatory network of plant thylakoid energy transduction. Trends Plant Sci 19:10–17

    Article  CAS  PubMed  Google Scholar 

  • Tikkanen M, Mekala N, Aro EM (2014) Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215

    Article  CAS  PubMed  Google Scholar 

  • Tikkanen M, Rantala S, Aro EM (2015) Electron flow from PSII to PSI under high light is controlled by PGR5 but not by PSBS. Front Plant Sci 6:521

    Article  PubMed  PubMed Central  Google Scholar 

  • Vass I (2011) Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. Physiol Plant 142:6–16

    Article  CAS  PubMed  Google Scholar 

  • Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu Rev Plant Biol 67:81–106

    Article  CAS  PubMed  Google Scholar 

  • Yamori W, Makino A, Shikanai T (2016) A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Sci Rep 6:20147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang SP, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis. Plant Cell Physiol 45:1595–1602

    Article  CAS  PubMed  Google Scholar 

  • Zivcak M, Brestic M, Kalaji HM, Govindjee (2014) Photosynthetic responses of sun- and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light? Photosynth Res 119:339–354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zivcak M, Brestic M, Kunderlikova K, Sytar O, Allakhverdiev SI (2015) Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves. Photosynth Res 126:449–463

    Article  CAS  PubMed  Google Scholar 

  • Zulfugarov IS, Tovuu A, Eu YJ, Dogsom B, Poudyal RS, Nath K, Hall M, Banerjee M, Yoon UC, Moon YH, An G, Jansson S, Lee CH (2014) Production of superoxide from Photosystem II in a rice (Oryza sativa L.) mutant lacking PsbS. BMC Plant Biol 14:242

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant 31300332 and 31670343), and an open fund from Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences.

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Authors and Affiliations

  1. Key Laboratory of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, Yunnan, China

    Wei Huang, Ying-Jie Yang, Hong Hu & Shi-Bao Zhang

  2. Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, 666303, Yunnan, China

    Wei Huang & Jiao-Lin Zhang

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  1. Wei Huang
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  2. Ying-Jie Yang
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  4. Hong Hu
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  5. Shi-Bao Zhang
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Correspondence to Shi-Bao Zhang.

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Huang, W., Yang, YJ., Zhang, JL. et al. Superoxide generated in the chloroplast stroma causes photoinhibition of photosystem I in the shade-establishing tree species Psychotria henryi . Photosynth Res 132, 293–303 (2017). https://doi.org/10.1007/s11120-017-0389-4

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